Award Abstract # 1533672
NCS-FO: The Structure of Neural Variability During Motor Learning

NSF Org: BCS
Division of Behavioral and Cognitive Sciences
Recipient: CARNEGIE MELLON UNIVERSITY
Initial Amendment Date: August 10, 2015
Latest Amendment Date: October 12, 2016
Award Number: 1533672
Award Instrument: Standard Grant
Program Manager: Kenneth Whang
BCS
 Division of Behavioral and Cognitive Sciences
SBE
 Directorate for Social, Behavioral and Economic Sciences
Start Date: September 1, 2015
End Date: August 31, 2020 (Estimated)
Total Intended Award Amount: $868,952.00
Total Awarded Amount to Date: $868,952.00
Funds Obligated to Date: FY 2015 = $868,952.00
History of Investigator:
  • Steven Chase (Principal Investigator)
    schase@cmu.edu
  • Byron Yu (Co-Principal Investigator)
  • Aaron Batista (Co-Principal Investigator)
Recipient Sponsored Research Office: Carnegie-Mellon University
5000 FORBES AVE
PITTSBURGH
PA  US  15213-3890
(412)268-8746
Sponsor Congressional District: 12
Primary Place of Performance: Carnegie-Mellon University
5000 Forbes Avenue
Pittsburgh
PA  US  15213-2685
Primary Place of Performance
Congressional District:
12
Unique Entity Identifier (UEI): U3NKNFLNQ613
Parent UEI: U3NKNFLNQ613
NSF Program(s): EFRI Research Projects,
IntgStrat Undst Neurl&Cogn Sys
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 8551, 8089, 8091
Program Element Code(s): 763300, 862400
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.075

ABSTRACT

Movements are inherently variable: one never throws a dart or a basketball in exactly the same way twice. On the face of it, this variability in behavior is detrimental to performance, preventing one from consistently hitting the bull's-eye or making the basket. However, computational theories posit that motor variability may also serve a functional role, enabling exploration and learning of more efficient movements. This creates an intriguing duality: while variability should be minimized for short-term motor performance (to act reliably), it should be maximized for long-term performance (to promote learning). During practice, variability might be useful for developing motor skill. When it's game time, however, variability should be suppressed to the greatest extent possible. Might the central nervous system set the amount of variability in a context-appropriate fashion? This study will investigate the neural correlates of motor variability and establish the connections between neural variability, behavioral performance, and learning.

Neural variability lies at the heart of several theoretical computational models, from implementations of probabilistic computation to Hebbian learning rules. Although the importance of variability has been well recognized, the structure and regulation of neural variability within the central nervous system is not well understood. This project coordinates a program of experiments and new analytical techniques to examine the structure of neural variability in the motor system. It seeks to establish, first, how variability depends on behavioral demands, and second, how variability impacts learning. To achieve this, many neurons of the motor and premotor cortices will be studied simultaneously during performance of demanding behaviors. By studying two distinct areas in the motor pathway, the impacts of noise on motor planning and execution can be examined separately. Furthermore, population recordings can be leveraged to decompose variability into three conceptually distinct components: (1) variability that is related to the task (signal variability), (2) trial-to-trial variability shared among neurons, and (3) private variability within each neuron. The investigators will explore how variability of each type is modulated by task context and learning. These decompositions will yield insight into the mechanisms of variability generation during performance.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 17)
Bittner SR, Williamson RC, Snyder AC, Litwin-Kumar A, Doiron B, *Chase SM, *Smith MA, and *Yu BM "Population activity structure of excitatory and inhibitory neurons." PLOS One , v.12 , 2017 , p.e0181773
Cowley, Benjamin R. AND Smith, Matthew A. AND Kohn, Adam AND Yu, Byron M. "Stimulus-Driven Population Activity Patterns in Macaque Primary Visual Cortex" PLOS Computational Biology , v.12 , 2016 , p.1-31 10.1371/journal.pcbi.1005185
Cowley BR, Snyder AC, Acar K, Williamson RC, Yu BM, Smith MA "Slow drift in neural activity as a signature of impulsivity in macaque visual and prefrontal cortex" Neuron , v.108 , 2020 , p.551
Cowley BR, Williamson RC, Acar K, *Smith MA and *Yu BM "Adaptive stimulus selection for optimizing neural population responses" Advances in Neural INformation Processing Systems , v.30 , 2017 , p.1395
+Degenhart AD, +Bishop WE, Oby ER, Tyler-Kabara EC, *Chase SM, *Batista AP, *Yu BM "Stabilization of a brain-computer interface via the alignment of low-dimensional spaces of neural activity" Nature Biomedical Engineering , v.4 , 2020 , p.672
Golub MD, Sadtler PT, Oby ER, Quick KM, Ryu SI, Tyler-Kabara EC, Batista AP, *Chase SM, and *Yu BM "Learning by neural reassociation" Nature Neuroscience , v.21 , 2018 , p.607
Hennig JA, Golub MD, Lund PJ, Sadtler PT, Oby ER, Quick KM, Ryu SI, Tyler-Kabara EC, *Batista AP, *Yu BM, *Chase SM "Constraints on neural redundancy" eLife , 2018
Jane E. Huggins and Christoph Guger and Mounia Ziat and Thorsten O. Zander and Denise Taylor and Michael Tangermann and Aureli Soria-Frisch and John Simeral and Reinhold Scherer and Rüdiger Rupp and Giulio Ruffini and Douglas K. R. Robinson and Nick F. Ra "Workshops of the Sixth International Brain?Computer Interface Meeting: brain?computer interfaces past, present, and future" Brain-Computer Interfaces , v.4 , 2017 , p.3-36 10.1080/2326263X.2016.1275488
Kohn A, Jasper AI, Semedo JD, Gokcen E, Machens CK, Yu BM "Principles of corticocortical communication: proposed schemes and design considerations" Trends Neurosci , v.43 , 2020 , p.725
Oby ER, Golub MD, Hennig JA, Degenhart AD, Tyler-Kabara EC, *Yu BM, *Chase SM, *Batista AP "New neural activity patterns emerge with long-term learning" PNAS , v.116 , 2019 , p.15210
Rasmussen, Robert G and Schwartz, Andrew and Chase, Steven M "Dynamic range adaptation in primary motor cortical populations" eLife , v.6 , 2017 , p.e21409 10.7554/eLife.21409
(Showing: 1 - 10 of 17)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Movements are inherently variable: whenever we throw a dart or a basketball, we never do so in the same way twice. On the face of it, this variability in behavior is detrimental to performance, as it prevents us from consistently hitting the bull’s eye or making the basket. However, computational theories posit that motor variability may also serve a functional role, allowing us to explore and learn more efficient movements. This creates an intriguing duality: while variability should be minimized for short-term motor performance (to act reliably), it should be maximized for long-term performance (to promote learning). During practice, variability might be useful for developing motor skill. When it’s game time, however, variability should be suppressed to the greatest extent possible. In this project, we investigated two questions on this theme. (1) Does the central nervous system regulate motor variability in a context-appropriate fashion? (2) Does neural variability regulate learning? Our investigation of these questions uncovered two central new discoveries.

First, we established that motor variability in non-human primates is regulated by reward in the same way that it is for humans: as incentives increase, behavioral performance also increases, but only up to a point. As rewards get too large, performance paradoxically decreases. Our finding is the first to show that animals can “choke under pressure,” just as humans do. By establishing an animal model of this behavior, we can now investigate the neural mechanisms that lead to reward-mediated performance variability.

Second, we discovered that long-term training can fundamentally alter neural variability by enabling the brain to produce new neural activity patterns. These new patterns are causally related to producing new abilities. Our finding lends support for different mechanisms of learning that may regulate neural variability over short- and long-timescales.

In terms of broader impacts, our work has provided training opportunities for 11 separate students and post-doctoral scholars. These trainees all received cross-disciplinary training in neurophysiology, statistics, and machine learning. In addition, we used funds from this grant to host a workshop open to the community on the neuroscience of learning. Finally, this grant helped support the development of new brain-computer interface algorithms that help paralyzed individuals gain control of prosthetic devices through the volitional modulation of neural activity.

 


Last Modified: 11/30/2020
Modified by: Steven M Chase

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